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Showing papers in "American Journal of Primatology in 2006"


Journal ArticleDOI
TL;DR: The data suggest that the reliability of a given fecal glucocorticoid assay in reflecting activity of the HPA axis in primates clearly depends on the species in question, and group‐specific assays have a high potential for cross‐species application.
Abstract: Most studies published to date that used fecal glucocorticoid measurements to assess adrenocortical activity in primate (and many nonprimate) species applied a specific cortisol or corticosterone assay However, since these native glucocorticoids are virtually absent in the feces of most vertebrates, including primates, the validity of this approach has recently been questioned Therefore, the overall aim of the present study was to assess the validity of four enzymeimmunoassays (EIAs) using antibodies raised against cortisol, corticosterone, and reduced cortisol metabolites (two group-specific antibodies) for assessing adrenocortical activity using fecal glucocorticoid metabolite (GCM) measurements in selected primate species (marmoset, long-tailed macaque, Barbary macaque, chimpanzee, and gorilla) Using physiological stimulation of the hypothalamo-pituitary-adrenocortical (HPA) axis by administering exogenous ACTH or anesthesia, we demonstrated that at least two assays detected the predicted increase in fecal GCM levels in response to treatment in each species However, the magnitude of response varied between assays and species, and no one assay was applicable to all species While the corticosterone assay generally was of only limited suitability for assessing glucocorticoid output, the specific cortisol assay was valuable for those species that (according to high-performance liquid chromatography (HPLC) analysis data) excreted clearly detectable amounts of authentic cortisol into the feces In contrast, in species in which cortisol was virtually absent in the feces, group-specific assays provided a much stronger signal, and these assays also performed well in the other primate species tested (except the marmoset) Collectively, the data suggest that the reliability of a given fecal glucocorticoid assay in reflecting activity of the HPA axis in primates clearly depends on the species in question Although to date there is no single assay system that can be used successfully across species, our data suggest that group-specific assays have a high potential for cross-species application Nevertheless, regardless of which GC antibody is chosen, our study clearly reinforces the necessity of appropriately validating the respective assay system before it is used Am J Primatol 68:257–273, 2006 © 2006 Wiley-Liss, Inc

210 citations


Journal ArticleDOI
TL;DR: Differences in these two sites' interaction patterns included bite rates, the role of food in aggressive interactions, and the context in which the interactions took place and are interpreted as resulting from differences in macaque species and behaviors, and human demography, culture, and behavioral patterns.
Abstract: An in-depth understanding of the contexts and patterns of human-macaque interactions can play an important role in assessing and managing the potential for pathogen transmission. The Padangtegal Monkey Forest in Bali, Indonesia, and the Upper Rock Nature Reserve in Gibraltar are two sites that have been relatively well studied in regard to human-macaque interactions. This article presents an overview of interaction patterns between humans and macaques at these sites along with a description of the cultural, demographic, and contextual differences between local and nonlocal humans at the sites. Differences in these two sites' interaction patterns included bite rates, the role of food in aggressive interactions, and the context in which the interactions took place. Similarities included overrepresentation by adult male macaques in interactions and a substantial impact by local cultural and demographic factors. These similarities and differences are interpreted as resulting from differences in macaque species and behaviors, and human demography, culture, and behavioral patterns.

174 citations


Journal ArticleDOI
TL;DR: Data is added to the database on intergroup coalitionary aggression in chimpanzees by describing three fatal attacks on adult males, plus a fourth attack on an adult male and an attack on a juvenile that were almost certainly fatal.
Abstract: Chimpanzees (Pan troglodytes) have hostile intergroup relations throughout most or all of their geographic range. Hostilities include aggressive encounters between members of neighboring communities during foraging and during patrols in which members of one community search for neighbors near territory boundaries. Attacks on neighbors involve coalitions of adult males, and are sometimes fatal. Targets include members of all age/sex classes, but the risk of lethal intergroup coalitionary aggression is highest for adult males and infants, and lowest for sexually swollen females. The best-supported adaptive explanation for such behavior is that fission-fusion sociality allows opportunities for low-cost attacks that, when successful, enhance the food supply for members of the attackers' community, improve survivorship, and increase female fertility. We add to the database on intergroup coalitionary aggression in chimpanzees by describing three fatal attacks on adult males, plus a fourth attack on an adult male and an attack on a juvenile that were almost certainly fatal. Observers saw four of these attacks and inferred the fifth from forensic and behavioral evidence. The attackers were males in two habituated, unprovisioned communities (Ngogo and Kanyawara) in Kibale National Park, Uganda. We also summarize data on other intercommunity attacks at Ngogo. Our observations are consistent with the "imbalance of power" hypothesis [Manson & Wrangham, Current Anthropology 32:369-390, 1991] and support the argument that lethal coalitionary intergroup aggression by male chimpanzees is part of an evolved behavioral strategy.

163 citations


Journal ArticleDOI
TL;DR: Social system correlations support the idea that there is an olfactory dimension to the concept of the social brain, using phylogenetic analysis of comparative volumetric data.
Abstract: Primates are usually thought of as "visual" mammals, and several comparative studies have emphasized the role of vision in primate neural and sociocognitive specialization. Here I explore the role of olfactory systems, using phylogenetic analysis of comparative volumetric data. The relative sizes of the main olfactory bulb (MOB) and accessory olfactory bulb (AOB) tend to show different evolutionary patterns in accordance with their different functions. Although there is some evidence of correlated evolution of the two systems, this is apparent in only one clade (the strepsirhines). As predicted, the MOBs correlate predominantly with ecological factors (activity period and diet), while the AOBs correlate with social and mating systems. Related olfactory structures (i.e., the piriform cortex and amygdala) exhibit correlated evolution with the AOBs but not with the MOBs, and the corticobasolateral part of the amygdala exhibits a correlation with social group size in platyrrhines similar to that observed for the AOB. These social system correlations support the idea that there is an olfactory dimension to the concept of the social brain.

141 citations


Journal ArticleDOI
TL;DR: In this paper, the authors analyzed grooming distribution among wild female Japanese macaques living in two groups on Yakushima and found that grooming was highly reciprocated (i.e., exchanged in kind) and directed up the hierarchy in both groups.
Abstract: Social primates spend a significant proportion of their time exchanging grooming with their group companions. Although grooming is mainly exchanged in kind, given its hygienic and tension-reducing functions, it is still debated whether grooming also provides some social benefits, such as preferential access to resources (e.g., food or mating partners). In this study we analyzed grooming distribution among wild female Japanese macaques living in two groups on Yakushima. We tested the tendency of monkeys to reciprocate the amount of grooming received, and to direct their grooming up the hierarchy. Then we analyzed the relation of grooming to three of its possible benefits: reduced aggression, increased tolerance over food, and agonistic support against a male aggressor. The data were analyzed by means of row-wise matrix correlations. Grooming was highly reciprocated (i.e., exchanged in kind) and directed up the hierarchy in both the study groups. No significant relationship was found between grooming and aggression. Conversely, grooming favored tolerance over food, since it was positively correlated with presence on the same food patch, close proximity, and close approaches (both within 1 m) during feeding. Grooming was also positively related to agonistic support against adult males, although this relationship became nonsignificant when we controlled for kinship. Although these results are not definitive, they suggest that monkeys may derive various social benefits from grooming. This conclusion is supported by the fact that in various primate species animals tend to prefer high-ranking individuals as grooming partners.

126 citations


Journal ArticleDOI
TL;DR: The results of this study suggest that female facial coloration may serve an alternative purpose to that of attracting males, and that the signal function of sexual skin and the intended recipients may vary across anatomical regions.
Abstract: Pink-to-red anogenital and facial sexual skin occurs in females of many primate species. Since female sexual skin color varies with reproductive state, it has long been assumed that color acts to stimulate male sexual interest. Although there is supportive evidence for this as regards anogenital skin, it is unclear whether this is also the case for facial sexual skin. In this study we experimentally manipulated digital facial and hindquarter images of female rhesus macaques (Macaca mulatta) for color within the natural range of variation. The images were presented to adult male conspecifics to assess whether the males exhibited visual preferences for red vs. non-red female coloration, and whether preferences varied with anatomical region. The males displayed significantly longer gaze durations in response to reddened versions of female hindquarters, but not to reddened versions of faces. This suggests that female facial coloration may serve an alternative purpose to that of attracting males, and that the signal function of sexual skin and the intended recipients may vary across anatomical regions.

119 citations


Journal ArticleDOI
TL;DR: It is speculated that interactions with humans may be linked to the observed patterns of infections, and hence that understanding the ecology of infectious diseases in nonhuman primates is of paramount importance for conservation and potentially for human‐health planning.
Abstract: Humans are responsible for massive changes to primate habitats, and one unanticipated consequence of these alterations may be changes in host-parasite interactions. Edges are a ubiquitous aspect of human disturbance to forest landscapes. Here we examine how changes associated with the creation of edges in Kibale National Park, Uganda, alter the parasite community that is supported by two species of African colobines: the endangered red colobus (Piliocolobus tephrosceles) and the black-and-white colobus (Colobus guereza). An analysis of 822 fecal samples from edge and forest interior groups revealed no difference in the richness of parasite communities (i.e., the number of parasite species recovered from the host's fecal sample). However, for both species the proportion of individuals with multiple infections was greater in edge than forest interior groups. The prevalence of specific parasites also varied between edge and forest interior groups. Oesophagostomum sp., a potentially deleterious parasite, was 7.4 times more prevalent in red colobus on the edge than in those in the forest interior, and Entamoeba coli was four times more prevalent in red colobus on the edge than in animals from the forest interior. Environmental contamination with parasites (measured as parasite eggs/gm feces) by red colobus from the edge and forest interior differed in a similar fashion to prevalence for red colobus, but it did not differ for black-and-white colobus. For example, egg counts of Oesophagostomum sp. were 10 times higher in red colobus from the edge than in those from the interior. The less severe infections in the black-and-white colobus relative to the red colobus may reflect the fact that black-and-white colobus raid agricultural crops while red colobus do not. This nutritional gain may facilitate a more effective immune response to parasites by the black-and-white colobus. The fact that animals on the edge are likely not nutritionally stressed raises an intriguing question as to what facilitates the elevated infections in edge animals. We speculate that interactions with humans may be linked to the observed patterns of infections, and hence that understanding the ecology of infectious diseases in nonhuman primates is of paramount importance for conservation and potentially for human-health planning.

115 citations


Journal ArticleDOI
TL;DR: This article found that the behavior of the partner in an unequal reward situation did not affect overall success rates, while pairs that had a tendency to alternate which individual received the higher value food in unequal reward situations were more than twice as successful in obtaining rewards than pairs in which one individual dominated the higher-value food.
Abstract: It was recently demonstrated that capuchin monkeys notice and respond to distributional inequity, a trait that has been proposed to support the evolution of cooperation in the human species. However, it is unknown how capuchins react to inequitable rewards in an unrestricted cooperative paradigm in which they may freely choose both whether to participate and, within the bounds of their partner's behavior, which reward they will receive for their participation. We tested capuchin monkeys with such a design, using a cooperative barpull, which has been used with great success in the past. Contrary to our expectations, the equity of the reward distribution did not affect success or pulling behavior. However, the behavior of the partner in an unequal situation did affect overall success rates: pairs that had a tendency to alternate which individual received the higher-value food in unequal reward situations were more than twice as successful in obtaining rewards than pairs in which one individual dominated the higher-value food. This ability to equitably distribute rewards in inherently biased cooperative situations has profound implications for activities such as group hunts, in which multiple individuals work together for a single, monopolizable reward.

115 citations


Journal ArticleDOI
TL;DR: Keystone habitats for forest frugivores are identified and results are discussed with reference to previous studies on this genus, and the importance of considering keystone habitats and local habitat diversity within the management of forestry concessions in the region is considered.
Abstract: Data are presented regarding the habitat use and ranging behavior of a spider monkey (Ateles chamek) community at Lago Caiman in northeastern Bolivia. Habitat use was driven primarily by fruit availability and distribution across the community home range. Strong seasonal variations occurred in fruit availability within all five of the floristically and phenologically distinct habitat types identified within the study site, and the spider monkeys dramatically shifted their ranging according to which habitat was richest in fleshy fruits. This use of local habitat diversity resulted in an unusually elongated shape for the home range that was otherwise typical of previous Ateles studies in terms of size. Ranging behavior was clumped and community core areas shifted seasonally across the focal community home range. Individual core areas were not relevant to the study due to dramatic community-wide shifts in ranging patterns. Day journey lengths were highly variable (460-5,690 m) and the distribution and abundance of fleshy fruit resources explained 81% of the monthly variations in mean day journey length. Keystone habitats for forest frugivores are identified and results are discussed with reference to previous studies on this genus, and the importance of considering keystone habitats and local habitat diversity within the management of forestry concessions in the region. Results are also discussed with reference to the behavioral ecology of the genus Ateles.

111 citations


Journal ArticleDOI
TL;DR: The suitability of gibbon songs are reassessed as a means of estimating the density and size of gibbons populations, and the proximate causes for the absence of duetting in silvery gibbons are discussed.
Abstract: Hardly any behavioral data are available for the silvery gibbon (Hylobates moloch), an endangered primate that is endemic to the island of Java, Indonesia. We studied the singing behavior of the easternmost population of this species in the Dieng mountains, central Java, in 1998-1999. We aimed to document the timing of singing, quantify the amount of singing by the respective sexes, and explore the role of bioacoustics in density estimation. A total of 122 song bouts in at least 12 groups were monitored. No duet songs were heard. Most of the song bouts (91.5%) were female solo song bouts or female scream bouts. In contrast to an earlier study on the westernmost population of silvery gibbons, during which few if any male songs were heard, at least 8.5% of the song bouts in our study were male solo song bouts. They were significantly longer in duration than the female songs. All male song bouts uttered before dawn (0520 hr) were produced in a chorus fashion, with at least three individuals participating. Choruses occurred about once every 8.5 days, and lasted longer and occurred earlier than female solo song bouts. Most male songs (60%) started between 0355-0440 hr, when it was still dark. All female songs, in contrast, started after 0500 hr, and female singing activity peaked around 0600. Regular male singing, male chorusing, and regular predawn singing have not previously been reported for silvery gibbons. Similarly separated periods of male and female solo songs and the absence of duetting have been observed in Kloss's gibbons (H. klossii) on the Mentawai Islands, and may represent synapomorphies shared by both species. The pronounced individual-specific song characteristics of silvery gibbons allow accurate mapping of groups. The density of gibbons 2 at our study site was established to be 1.9-3.7 groups/km, corresponding to 6.7-13.1 individuals/km(2). We reassess the suitability of gibbon songs as a means of estimating the density and size of gibbon populations, and discuss the proximate causes for the absence of duetting in silvery gibbons. The abstract will be available at the website.

108 citations


Journal ArticleDOI
TL;DR: This is one of the first data sets to objectively demonstrate that PRT for voluntary presentation of IM injections of anesthetic can significantly affect some of the physiological measures correlated with stress responses to chemical restraint in captive chimpanzees.
Abstract: Positive reinforcement training (PRT) techniques have received considerable attention for their stress reduction potential in the behavioral management of captive nonhuman primates. However, few published empirical studies have provided physiological data to support this position. To address this issue, PRT techniques were used to train chimpanzees (Pan troglodytes) to voluntarily present a leg for an intramuscular (IM) injection of anesthetic. Hematology and serum chemistry profiles were collected from healthy chimpanzees (n=128) of both sexes and various ages during their routine annual physical examinations over a 7-year period. Specific variables potentially indicative of acute stress (i.e., total white blood cell (WBC) counts, absolute segmented neutrophils (SEG), glucose (GLU) levels, and hematocrit (HCT) levels) were analyzed to determine whether the method used to administer the anesthetic (voluntary present for injection vs. involuntary injection) affected the physiological parameters. Subjects that voluntarily presented for an anesthetic injection had significantly lower mean total WBC counts, SEG, and GLU levels than subjects that were involuntarily anesthetized by more traditional means. Within-subjects analyses revealed the same pattern of results. This is one of the first data sets to objectively demonstrate that PRT for voluntary presentation of IM injections of anesthetic can significantly affect some of the physiological measures correlated with stress responses to chemical restraint in captive chimpanzees.

Journal ArticleDOI
TL;DR: This study shows that tamarins have greater vocal control in the context of auditory feedback perturbation than previously suspected.
Abstract: The Lombard effect-an increase in vocalization amplitude in response to an increase in background noise-is observed in a wide variety of animals. We investigated this basic form of vocal control in the cotton-top tamarin (Saguinus oedipus) by measuring the amplitude of a contact call, the combination long call (CLC), while simultaneously varying the background noise level. All subjects showed a significant increase in call amplitude and syllable duration in response to an increase in background noise amplitude. Together with prior results, this study shows that tamarins have greater vocal control in the context of auditory feedback perturbation than previously suspected.

Journal ArticleDOI
TL;DR: This unique data set adds to knowledge about the nutritional composition of foods eaten by gorillas across habitats, is useful for understanding aspects of feeding behavior, and provides valuable comparative data for optimizing the diets of gorillas ex situ.
Abstract: Foods eaten by gorillas (Gorilla beringei) in Bwindi Impenetrable National Park (BINP), Uganda, were analyzed for their nutrient content. The goal of the study was to assess the amounts of fiber, protein, and sugars in the foods eaten by the Bwindi gorillas, and to determine whether condensed tannins and cyanide are present in these foods. A total of 127 food plant parts representing 84 plant species eaten by two groups of Bwindi gorillas were collected, processed, and analyzed for their chemical contents. The Bwindi gorilla ate foods that contain 2–28% crude protein (CP), 21–88% neutral detergent fiber (NDF), 14–60% acid detergent fiber (ADF), 2–42% acid detergent lignin (ADL), and ≤1–50% water-soluble carbohydrates (WSC) on a dry matter (DM) basis. Moisture in these foods ranged from 7% to 96%. Approximately 35% of the foods analyzed contained condensed tannins, and two foods contained cyanogenic glycosides. This is the first detailed report regarding the nutritional chemistry of gorilla foods in Bwindi, many of which are also eaten by other primates. This unique data set adds to our knowledge about the nutritional composition of foods eaten by gorillas across habitats, is useful for understanding aspects of feeding behavior, and provides valuable comparative data for optimizing the diets of gorillas ex situ. Am. J. Primatol. 68:1–17, 2006. © 2005 Wiley-Liss, Inc.

Journal ArticleDOI
TL;DR: This special issue emerged from a symposium held during the 20th Congress of the International Primatological Society in Torino, Italy, in August 2004 and reflects a surge of interest in diverse aspects of olfaction–an interest that has been stimulated by the more rigorous theoretical approaches and new techniques that recently become available.
Abstract: This special issue emerged from a symposium held during the 20th Congress of the International Primatological Society in Torino, Italy, in August 2004. The symposium brought together scientists studying several different aspects of olfaction in primates. The topics addressed ranged from the morphology and physiology of the sensory apparatus, the genetics and chemistry of olfactory signals and the use of such signals in primate communication, to a comparative analysis of the role of olfaction in neural evolution. The papers in this issue reflect a surge of interest in diverse aspects of olfaction–an interest that has been stimulated by the more rigorous theoretical approaches and new techniques that have recently become available. This introduction briefly reviews past research on primate olfaction, summarizes the scope of this special issue, and provides a somewhat speculative glimpse of the future. Am. J. Primatol. 68:519–524, 2006.© 2006 Wiley-Liss, Inc.

Journal ArticleDOI
TL;DR: The selection index of tree species for lichens was positively related to lichen coverage per branch on tree species, demonstrating that the monkeys preferred tree species with abundant lichens, as well as dead trees forLichens.
Abstract: We studied the diet and food availability of a group of Sichuan snub-nosed monkeys for 14 months (July 2003 to September 2004, except for February) in the Shennongjia Nature Reserve, China. This species is primarily a lichen eater, with lichens (Usneaceae) accounting for 43.28% of feeding records (n=3,452). Other food types in the diet were young leaves (28.71%), fruits or seeds (14.57%), buds (5.36%), mature leaves (3.51%), herbs (2.09%), bark (1.36%), and flowers (1.13%). The monkeys used 23 plant species. Their diet showed a complicated seasonal variation: the monthly diet varied from primarily lichens in November-April, to a mixture of leaves and lichens in May-July, to a mixture of fruits or seeds and lichens in August-October (the latter depended on annual fruit and seed availability). The proportion of fruits or seeds in the diet was negatively correlated with that of lichens, which suggests that the monkeys prefer fruits or seeds to lichens when all of these items are available. The fruit or seed availability varied greatly between the two study years. The proportion of lichens, young leaves, flowers, and fruits or seeds in the diet was positively associated with their availability. The monkeys appeared to be selective feeders. They preferred 10 tree species for plant parts, and nine tree species for lichens. The selection index of tree species for lichens was positively related to lichen coverage per branch on tree species, demonstrating that the monkeys preferred tree species with abundant lichens, as well as dead trees for lichens. The results suggest that dead-tree harvesting in the reserve could significantly reduce the quality of habitat for these monkeys, and should therefore be prohibited. Connus controversa, Cerasus discadenia, Salix willichiana, and Malus halliana should be conserved as top priority species because the monkeys preferred them for both their vegetative parts and the lichens that grow on them.

Journal ArticleDOI
TL;DR: A risk assessment model is developed to describe the likelihood of cross‐species transmission of simian foamy virus (SFV) from temple macaques (Macaca fascicularis) to visitors at monkey temples in Asia, creating the potential for NHP–human disease transmission.
Abstract: Contact between humans and nonhuman primates (NHPs) frequently occurs at monkey temples (religious sites that have become associated with free-ranging populations of NHPs) in Asia, creating the potential for NHP-human disease transmission. In March 2003 a multidisciplinary panel of experts participated in a workshop designed to model the risk of NHP-human pathogen transmission. The panel developed a risk assessment model to describe the likelihood of cross-species transmission of simian foamy virus (SFV) from temple macaques (Macaca fascicularis) to visitors at monkey temples. SFV is an enzootic simian retrovirus that has been shown to be transmitted from NHPs to humans. In operationalizing the model field data, laboratory data and expert opinions were used to estimate the likelihood of SFV transmission within this context. This model sets the stage for a discussion about modeling as a risk assessment tool and the kinds of data that are required to accurately predict transmission.

Journal ArticleDOI
TL;DR: This paper reviews recent findings on scent‐marking behavior in wild New World primates and examines three functional hypotheses: territoriality, regulation of social and reproductive dominance, and mating competition/mate attraction to suggest a hypothesized function in intrasexual competition and intersexual mate choice.
Abstract: This paper reviews recent findings on scent-marking behavior in wild New World primates. These findings are used to examine three functional hypotheses: territoriality, regulation of social and reproductive dominance, and mating competition/mate attraction. Available data provide little evidence for a territorial function of scent-marking behavior in New World primates. Evidence for a function in the regulation of social and reproductive dominance is ambiguous. The patterns of scent marking found so far (i.e., rates of scent marking according to sex and social or reproductive status, and the spatial distribution of scent marks), and the sparse information on responses to scent marks are consistent with a hypothesized function in intrasexual competition and intersexual mate choice. Suggestions for future research are made.

Journal ArticleDOI
TL;DR: First evidence of intragroup coalitionary aggression leading to the death of a wild young adult male spider monkey during a long‐term study of a well‐habituated community at the Otoch Ma'ax Yetel Kooh reserve in Yucatan, Mexico is reported.
Abstract: We report the first evidence of intragroup coalitionary aggression leading to the death of a wild young adult male spider monkey. During a long-term study of a well-habituated community at the Otoch Ma'ax Yetel Kooh reserve in Yucatan, Mexico, a young adult male sustained severe injuries repeatedly between January and March 2002. On 1 April 2002 the same male was the victim of an intragroup attack by at least one adult male that resulted in his death. We highlight several causes of intragroup aggression that may account for the killing.

Journal ArticleDOI
TL;DR: The overall results indicate that both gorillas and orangutans are sensitive to the attentional state of a human experimenter and use appropriate communicative signals to gain that individual's attention.
Abstract: In this study we investigated the communicative abilities of 10 orangutans (Pongo pygmaeus) and seven western lowland gorillas (Gorilla gorilla gorilla), and particularly focused on their sensitivity to the attentional state of a human experimenter when choosing from a repertoire of both auditory and visual communication strategies. In experiment 1 a banana was placed in front of the subject's cage and a human experimenter was either present or absent. The subject's behavior was recorded for 60 sec. Both gorillas and orangutans gestured (t(16)=-3.58, P<.005) and vocalized (t(16)=-2.47, P<.05) more when the experimenter was present. In experiment 2 a human experimenter held a banana in front of the subject's cage and was oriented either toward or away from the subject. Again the subject's behavior was recorded for 60 sec. In this experiment both gorillas and orangutans gestured significantly more frequently (t(16)=3.40, P<.005) when the experimenter was oriented toward them. In addition, gorillas and orangutans used other forms of visual communication signals, such as lip pout (t(16)=3.66, P<.005), barter/trade (t(16)=2.31, P<.05), and body present (t(16)=2.31, P<.05) significantly more when an experimenter was facing them. The overall results indicate that both gorillas and orangutans are sensitive to the attentional state of a human experimenter and use appropriate communicative signals to gain that individual's attention. These results are also similar to previous findings on communicative behaviors in chimpanzees.

Journal ArticleDOI
TL;DR: It is found that older infants were the most attentive and most socially‐influenced foragers among the three age categories in absolute terms, but were not more attentive than young infants given their low foraging activity.
Abstract: In this study we investigated the extent and pattern of social influences (i.e., the use of a conspecific as a model) on the foraging behavior of immature, wild common marmosets (Callithrix jacchus) as a function of the age of individuals. We compared the foraging activities and interactions with subadult and adult group members (older than 15 months) of young infants (1-2 months old), older infants (3-4 months old), and juveniles (5-10 months old). In addition to measuring the intensities of model-independent foraging (MIF) and merely paying attention to the model's foraging activities, we examined the frequencies of three types of model-dependent foraging (MDF): "follow the model", "manipulate the same object", and "forage together". We found that older infants were the most attentive and most socially-influenced foragers among the three age categories in absolute terms, but were not more attentive than young infants given their low foraging activity. Juveniles, in contrast, tended to have reduced overall foraging intensity compared to infants, but showed relatively more MDF in cases in which they observed subadult or adult models. Female models appeared to be more attractive than male models. These findings suggest that infants are generally more attentive to the foraging behavior of subadults and adults than juveniles, with the latter being more influenced when they had observed a model before. These subtle age-dependent effects of social foraging not only extend the assumption that young primates seek information from adults, they also suggest a complex interplay among physical and cognitive maturation, independence, and social dynamics.

Journal ArticleDOI
TL;DR: The investigation of the diet of wild chimpanzees may serve as a guideline to discovering plants with bioactive properties that should be preserved from destruction because of their health maintenance value for great ape populations.
Abstract: We examined the biological activities of a selected sample (84 crude extracts) of 24 species eaten by wild chimpanzees (Pan troglodytes schweinfurthii) in the Kibale National Park, western Uganda, to assess their potential chemotherapeutic values. Antibacterial, antimalarial, and/or antileishmania activities were observed in some crude extracts, and five of these extracts showed a significant cytotoxicity against humantumor cells. Active compounds isolated from three plant parts occasionally ingested by chimpanzees (Diospyros abyssinica (Ebenaceae) bark, Uvariopsis congensis (Annonaceae) leaves, and Trichilia rubescens (Meliaceae) leaves) showed highly significant medicinal properties. Two novel antiparasitic limonoids were isolated Trichilia rubescens and their molecular structures were determined. In addition to elucidating the natural equilibrium maintained between hosts and pathogens, our investigation of the diet of wild chimpanzees may serve as a guideline to discovering plants with bioactive properties that should bepreserved from destruction because of their health maintenance value for great ape populations

Journal ArticleDOI
TL;DR: The data suggest that colobus probably travel between fragments, and conservation efforts should focus on treating the small forests and their connecting areas as a single conservation unit.
Abstract: The Boabeng-Fiema Monkey Sanctuary (BFMS) is inhabited by a growing population of Ursine colobus (Colobus vellerosus), a species that is listed as vulnerable. Smaller, degraded forest fragments that surround the BFMS also contain C. vellerosus and may provide an important habitat for the monkeys. Our objectives were to 1) determine the current population size and density of C. vellerosus at BFMS and in five surrounding fragments, 2) examine the differences in demographics between the fragments and BFMS, and 3) determine whether a relationship exists between population density and fragment size and isolation distance from BFMS. The census was a complete count and was conducted for 1 month (July 2003) by S.W. and trained research assistants. Seven census routes were walked simultaneously on 13 days. The 2003 population estimate of C. vellerosus at BFMS was 217-241 individuals (15 groups), a slight increase from the 2000 census. Numbers in the fragments (58-62, six groups) have remained stable since 1997, when the only other census of these fragments was conducted. Mean group size did not differ between the fragments and BFMS. Larger fragments had larger numbers of colobus, but there was no relationship between fragment size and colobus density. Isolation distance had no effect on population density. Our data suggest that colobus probably travel between fragments. Conservation efforts should focus on treating the small forests and their connecting areas as a single conservation unit.

Journal ArticleDOI
TL;DR: Food availability was poor in summer and winter, but in several years the monkeys were able to consume nuts during those seasons, emphasizing the importance of conducting long‐term studies on both food availability and the food habits of animals in the temperate zone.
Abstract: We studied the relationship between the food habits of Japanese macaques (Macaca fuscata) and the availability of nuts (Fagus crenata, Zelkova serrata, Carpinus spp., and Torreya nucifera) on Kinkazan Island, northern Japan, from 1997 to 2005 to examine the long-term variations in both food habits and availability. The food habits of the monkeys showed clear seasonal changes: the staple foods were woody leaves and flowers in spring (May and June), woody leaves and seeds or fruits other than nuts in summer (July and August), nuts and seeds or fruits other than nuts in fall (September-November), and herbaceous plants in winter (December-April). The availability of nuts, combinations of masting species, and energy production varied among years. Food habits varied among years, but the magnitude of variability of food habits differed among seasons, with large variability during summer and winter, and small variability in spring. Food availability was poor in summer and winter, but in several years the monkeys were able to consume nuts during those seasons. We emphasize the importance of conducting long-term studies on both food availability and the food habits of animals in the temperate zone.

Journal ArticleDOI
TL;DR: A survey of behavioral data records spanning 44 years for health‐related data found a combination of standardized and nonstandardized data for the entire period, and describes how the current monitoring effort at Gombe was designed based on the findings.
Abstract: Disease outbreaks, either in isolation or in concert with other risk factors, can pose serious threats to the long-term persistence of mammal populations, and these risks become elevated as population size decreases and/or population isolation increases. Many chimpanzee study sites are increasingly isolated by loss of habitat due to human encroachment, and managers of parks that contain chimpanzees perceive that disease outbreaks have been and continue to be significant causes of mortality for chimpanzees. Major epidemics at Gombe National Park include suspected polio in 1966; respiratory diseases in 1968, 1987, 1996, 2000, and 2002; and sarcoptic mange in 1997. These outbreaks have led park managers and researchers working in Gombe to conclude that disease poses a substantial risk to the long-term survival of Gombe's chimpanzee population. We surveyed behavioral data records spanning 44 years for health-related data and found a combination of standardized and nonstandardized data for the entire period. Here we present the types of data found during the survey, discuss the usefulness of these data in the context of risk assessment, and describe how our current monitoring effort at Gombe was designed based on our findings.

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TL;DR: A 9-month-long investigation of the feeding ecology of a troop of howler monkeys (n = 24) that have lived for the past 25 years in a 12-ha cacao plantation in the lowlands of Tabasco, Mexico as discussed by the authors.
Abstract: Recent evidence indicates that primate populations may persist in neotropical fragmented landscapes by using arboreal agroecosystems, which may provide temporary habitats, increased areas of vegetation, and connectivity, among other benefits. However, limited data are available on how primates are able to sustain themselves in such manmade habitats. We report the results of a 9-month-long investigation of the feeding ecology of a troop of howler monkeys (n = 24) that have lived for the past 25 years in a 12-ha cacao plantation in the lowlands of Tabasco, Mexico. A vegetation census indicated the presence of 630 trees (> or =20 cm diameter at breast height (DBH)) of 32 shade species in the plantation. The howlers used 16 plant species (13 of which were trees) as sources of leaves, fruits, and flowers. Five shade tree species (Ficus cotinifolia, Pithecellobium saman, Gliricidia sepium, F. obtusifolia, and Ficus sp.) accounted for slightly over 80% of the total feeding time and 78% of the total number trees (n = 139) used by the howlers, and were consistently used by the howlers from month to month. The howlers spent an average of 51% of their monthly feeding time exploiting young leaves, 29% exploiting mature fruit, and 20% exploiting flowers and other plant items. Monthly consumption of young leaves varied from 23% to 67%, and monthly consumption of ripe fruit varied from 12% to 64%. Differences in the protein-to-fiber ratio of young vs. mature leaves influenced diet selection by the monkeys. The howlers used 8.3 ha of the plantation area, and on average traveled 388 m per day in each month. The howlers preferred tree species whose contribution to the total tree biomass and density was above average for the shade-tree population in the plantation. Given the right conditions of management and protection, shaded arboreal plantations in fragmented landscapes can sustain segments of howler monkey populations for many decades.

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TL;DR: A definition of food quality is suggested that includes not only the amount of valuable food contents and the digestibility of different foods, but also the rate at which the food can be harvested and processed.
Abstract: Testing ecological or socioecological models in primatology often requires estimates of individual energy intake. It is a well established fact that the nutrient content (and hence the energy content) of primate food items is highly variable. The second variable in determining primate energy intake, i.e., the ingestion rate, has often been ignored, and few studies have attempted to estimate the relative importance of the two predictors. In the present study individual ingestion rates were measured in two ecologically very different populations of Hanuman langurs (Semnopithecus entellus) at Jodhpur, India, and Ramnagar, Nepal. Protein and soluble sugar concentrations in 50 and 100 food items. respectively, were measured using standardized methods. Variation in ingestion rates (gram of dry matter per minute) was markedly greater among food items than among langur individuals in both populations, but did not differ systematically among food item categories defined according to plant part and age. General linear models (GLMs) with ingestion rate, protein, and soluble sugar content explained 40-80% of the variation in energy intake rates (kJ/min). The relative importance of ingestion rates was either similar (Ramnagar) or much greater (Jodhpur) than the role of sugar and/or protein content in determining the energy intake rates of different items. These results may impact socioecological studies of variation in individual energy budgets, investigations of food choice in relation to chemical composition or sensory characteristics, and research into habitat preferences that measures habitat quality in terms of abundance of important food sources. We suggest a definition of food quality that includes not only the amount of valuable food contents (energy, vitamins, and minerals) and the digestibility of different foods, but also the rate at which the food can be harvested and processed. Such an extended definition seems necessary because time may constrain primates when feeding competition is intense and foraging is risk-prone.

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TL;DR: Three cases of coalitionary aggression by adult male black‐handed spider monkeys (Ateles geoffroyi) against subadult males within their community on Barro Colorado Island, Panama are reported, which suggests that intense competition among males for access to reproductively viable females may be a contributing factor.
Abstract: I report three cases of coalitionary aggression by adult male black-handed spider monkeys (Ateles geoffroyi) against subadult males within their community on Barro Colorado Island (BCI), Panama. Two of these cases were followed by the disappearance and presumed death of the victim. Similar behavior was recently reported by Valero et al. [in press], who suggested that this behavior may be the result of intense male reproductive competition. Like the single instance they reported, the cases I report all occurred when the operational sex ratio was approximately 1:1, which suggests that intense competition among males for access to reproductively viable females may be a contributing factor. Additionally the very low density of spider monkeys on BCI may play a significant role in the occurrence of this lethal aggression. Large numbers of adult males are not necessary to protect a territorial boundary against neighboring groups, and additional males may act merely as mating competition.

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TL;DR: Results suggest that Alouatta pigra individuals that lived near human settlements in Belize were infected with Giardia duodenalis, which is transmitted from people and/or domestic animals to A. pigra.
Abstract: Parasites are important members of the ecological web within which an animal lives, and can be used as indicators of ecosystem health. However, few baseline parasitological data are available for free-ranging animals, particularly for the black howler monkey (Alouatta pigra). In this study a total of 283 fecal samples were collected from 50 individually identified A. pigra during 2003 and 2004 and examined for parasites. The samples were processed using standard quantitative centrifugation concentration techniques, with sugar and zinc sulfate used as flotation media. The slides were examined using bright-field and phase microscopy. Antigen capture enzyme-linked immunosorbent assays (ELISAs) were used to detect protozoa. Four parasites were detected: 1) Controrchis biliophilus (Dicrocoeliidae), 2) Trypanoxyuris minutus (Oxyuridae), 3) Giardia sp. (Hexamitidae), and 4) Entamoeba sp. (Endamoebidae). Controrchis biliophilus was detected in 80% (wet season) and 81% (dry season) of the A. pigra samples; Trypanoxyuris minutus was detected in 8% (wet season) and 27% (dry season) of samples; and Giardia sp. was detected in 40% (wet season) and 27% (dry season) of samples. For the first time, DNA from Giardia sp.-positive fecal samples was extracted from A. pigra. Alouatta pigra individuals that lived near human settlements in Belize were infected with Giardia duodenalis (syn. G. lamblia, G. intestinalis) Assemblages A and B. These results suggest that G. duodenalis is transmitted from people and/or domestic animals to A. pigra.

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TL;DR: A core marker set of four multiplex polymerase chain reaction (PCR) panels comprising 15 autosomal short tandem repeat (STR) loci with high information content selected from existing panels of well‐characterized markers that are currently used for parentage assessment and genetic management of rhesus macaques is assembled.
Abstract: To preserve genetic variability and minimize genetic subdivision among captive Macaca mulatta at each of the U.S. National Institutes of Health (NIH)-sponsored regional research colonies, the genetic structure of each colony must be characterized. To compare population genetic and demographic parameters across colonies and generations, one standard panel of highly informative genetic markers is required. We assembled a core marker set of four multiplex polymerase chain reaction (PCR) panels comprising 15 autosomal short tandem repeat (STR) loci with high information content selected from existing panels of well-characterized markers that are currently used for parentage assessment and genetic management of rhesus macaques. We then assessed the effectiveness of these loci for providing high probabilities of individual identification and parentage resolution, and for estimating population genetic parameters that are useful for genetic management.

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TL;DR: The results show that diseases other than Ebola may also threaten wild great apes, and indicate that the role of anthrax in great ape mortality may have been underestimated, and suggest that risk identification, assessment, and management for the survival of the last great apes should be performed with an open mind.
Abstract: During the period of December 2004 to January 2005, Bacillus anthracis killed three wild chimpanzees (Pan troglodytes troglodytes) and one gorilla (Gorilla gorilla gorilla) in a tropical forest in Cameroon. While this is the second anthrax outbreak in wild chimpanzees, this is the first case of anthrax in gorillas ever reported. The number of great apes in Central Africa is dramatically declining and the populations are seriously threatened by diseases, mainly Ebola. Nevertheless, a considerable number of deaths cannot be attributed to Ebola virus and remained unexplained. Our results show that diseases other than Ebola may also threaten wild great apes, and indicate that the role of anthrax in great ape mortality may have been underestimated. These results suggest that risk identification, assessment, and management for the survival of the last great apes should be performed with an open mind, since various pathogens with distinct characteristics in epidemiology and pathogenicity may impact the populations. An animal mortality monitoring network covering the entire African tropical forest, with the dual aims of preventing both great ape extinction and human disease outbreaks, will create necessary baseline data for such risk assessments and management plans.